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The geographic mosaic of arms race coevolution is closely matched to prey population structure.

ABSTRACT: Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the geographic mosaic of arms race coevolution between resistant garter snakes (Thamnophis sirtalis) and toxic newts (Taricha granulosa). We found that predator resistance and prey toxin levels are functionally matched in co-occurring populations, suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic differentiation, showing a clear signature of adaptation to local toxin levels in newts. Contrastingly, newt toxin levels are best predicted by genetic differentiation among newt populations, and to a lesser extent, by the local environment and snake resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but prey population structure seems to be of particular influence on local phenotypic variation in both species throughout the geographic mosaic. Our results imply that processes other than reciprocal selection, like historical biogeography and environmental pressures, represent an important source of variation in the geographic mosaic of coevolution. Such a pattern supports the role of "trait remixing" in the geographic mosaic theory, the process by which non-adaptive forces dictate spatial variation in the interactions among species.

SUBMITTER: Hague MTJ

PROVIDER: S-EPMC7403720 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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The geographic mosaic of arms race coevolution is closely matched to prey population structure.

Hague Michael T J MTJ Stokes Amber N AN Feldman Chris R CR Brodie Edmund D ED Brodie Edmund D ED

Evolution letters 20200609 4

Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the ...[more]

PMID: 32774881

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Project description:The geographic mosaic theory of coevolution (GMC) posits that coevolutionary dynamics go beyond local coevolution and are comprised of the following three components: geographic selection mosaics, coevolutionary hot spots, and trait remixing. It is unclear whether the GMC applies to bacteria, as horizontal gene transfer and cosmopolitan dispersal may violate theoretical assumptions. Here, we test key GMC predictions in an antibiotic-producing bacterial symbiont (genus Pseudonocardia) that protects the crops of neotropical fungus-farming ants (Apterostigma dentigerum) from a specialized pathogen (genus Escovopsis). We found that Pseudonocardia antibiotic inhibition of common Escovopsis pathogens was elevated in A. dentigerum colonies from Panama compared to those from Costa Rica. Furthermore, a Panama Canal Zone population of Pseudonocardia on Barro Colorado Island (BCI) was locally adapted, whereas two neighboring populations were not, consistent with a GMC-predicted selection mosaic and a hot spot of adaptation surrounded by areas of maladaptation. Maladaptation was shaped by incongruent Pseudonocardia-Escovopsis population genetic structure, whereas local adaptation was facilitated by geographic isolation on BCI after the flooding of the Panama Canal. Genomic assessments of antibiotic potential of 29 Pseudonocardia strains identified diverse and unique biosynthetic gene clusters in BCI strains despite low genetic diversity in the core genome. The strength of antibiotic inhibition was not correlated with the presence/absence of individual biosynthetic gene clusters or with parasite location. Rather, biosynthetic gene clusters have undergone selective sweeps, suggesting that the trait remixing dynamics conferring the long-term maintenance of antibiotic potency rely on evolutionary genetic changes within already-present biosynthetic gene clusters and not simply on the horizontal acquisition of novel genetic elements or pathways.IMPORTANCE Recently, coevolutionary theory in macroorganisms has been advanced by the geographic mosaic theory of coevolution (GMC), which considers how geography and local adaptation shape coevolutionary dynamics. Here, we test GMC in an ancient symbiosis in which the ant Apterostigma dentigerum cultivates fungi in an agricultural system analogous to human farming. The cultivars are parasitized by the fungus Escovopsis The ants maintain symbiotic actinobacteria with antibiotic properties that help combat Escovopsis infection. This antibiotic symbiosis has persisted for tens of millions of years, raising the question of how antibiotic potency is maintained over these time scales. Our study tests the GMC in a bacterial defensive symbiosis and in a multipartite symbiosis framework. Our results show that this multipartite symbiotic system conforms to the GMC and demonstrate that this theory is applicable in both microbes and indirect symbiont-symbiont interactions.

Dataset Information

The geographic mosaic of arms race coevolution is closely matched to prey population structure.

Publications

The geographic mosaic of arms race coevolution is closely matched to prey population structure.

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